Edentates of the Saracá-Taquera National Forest, Pará, Brazil

(Cingulata: Dasypodidae). Acta Theriologica 46(1): 53 59. Ximenez, A. y Achaval, F. 1966. Sobre la presencia en el Uruguay del tatú de rabo molle, Cabassous tatouay (Desmarest) (Edentata, Dasypodidae). Com. Zool. Mus. Hist. Nat. Montevideo 9(109): 1 5. Edentates of the Saracá-Taquera National Forest, Pará, Brazil Leonardo de Carvalho Oliveira Sylvia Miscow Mendel, Diogo Loretto José de Sousa e Silva Júnior Geraldo Wilson Fernandes Introduction The order Xenarthra contains 31 living species distributed in 13 genera, all but one of which are restricted to the Neotropics (Wetzel, 1982; Fonseca and Aguiar, 2004). Nineteen of these species, distributed in ten genera and four families, can be found in Brazil (Fonseca et al., 1996). This order embodies a substantial amount of the evolutionary history of mammals (Fonseca, 2001) and is potentially a basal offshoot of the earliest placental mammals (Murphy et al., 2001). Despite their ecological importance and the need to highlight them in conservation programs, xenarthrans are virtually unstudied when compared with other, better-known mammals (Fonseca, 2001). At least 13 species of xenarthrans are found in the rainforests of Amazonia, four of which are endemic (Fonseca et al., 1996); another two are on the Brazilian Red List of threatened species (Fonseca and Chiarello, 2003). Although the Xenarthra include few species compared with other orders of Brazilian mammals, only a handful of field studies have focused on them, and their geographic distributions are still poorly known. Here we present data on the occurrence of xenarthrans in the Saracá-Taquera National Forest (STNF) in northwestern Pará, Brazil. Field Site and Methods The Saracá-Taquera National Forest (429,600 ha) is a bauxite-rich area immediately south of the village of Porto Trombetas (01 40 S, 56 00 W), in the municipality of Oriximiná in western Pará. Our study site in the STNF is about 100 km west of the confluence of the Rios Trombetas and Amazonas. The bauxite is mined by the Rio do Norte Mining Company (Mineração Rio do Norte MRN). The deposits are associated with a series of Tertiary boundaries, occurring in small plateaus at altitudes between 150 200 m. Mining bauxite on these plateaus involves the wholesale removal of the rainforest along with the first 4 15 m of soil. Heavy machinery works around the clock to extract the ore, which is the raw material for the production of aluminum. After an area has been mined out, the pits are filled with a mixture of soil and vegetative debris, and the area is replanted with native seedlings by the mining company. Our fieldwork for this study focused on three regions: the Almeidas plateau, which has been undergoing stepwise deforestation since 2002; in areas on the Saracá plateau, which was mined out and reforested during the 1980s and 1990s; and on sightings and road kills along a 30-km stretch of road between Porto de Trombetas and the Almeidas plateau (Fig. 1). From April 2002 to December 2004, a small team of three carried out ten field trips of 15 days each. On each field trip, the team was composed of two researchers (L. C. Oliveira and either S. M. Mendel or D. M. Loretto) plus a field assistant. Edentates were recorded whenever they were seen on trails in both mature forest and reforested areas. Additional records on the occurrence of edentates in the region were gathered from publications (Wetzel, 1982, 1985a, 1985b; Emmons and Feer, 1997; Eisenberg and Redford, 1999; Silva Júnior and Nunes, 2001; Silva Júnior et al., 2001) as well as two technical reports: the Saracá-Taquera National Forest Management Plan (STCP, 2001) and an environmental impact study (Brandt Meio Ambiente, 2001), as well as from specimens in the Museu Paraense Emílio Goeldi (MPEG), Belém. During our fieldwork in STNF we found 11 dead animals, which we compared directly with museum specimens at MPEG. We deposited tissue samples from the animals at the PUCMinas Natural History Museum, and also took reference photographs of live animals in the field. We interviewed four technicians from the Brazilian Institute of the Environment and Renewable Natural Resources (IBAMA) who were working in the region, and also ten of our local field assistants. We presented each interviewee with the illustrations of the Xenarthra from Emmons and Feer (1997), and asked them to identify those which they had seen in the region. For each sighting they reported, we noted the species, the type of record, and the location and estimated date of the sighting. We also asked to see any remains, such as the skulls and carapaces of animals which were either hunted or found dead. 3

FIGURE 1. Map of the Saracá-Taquera National Forest with the study areas represented. Results Based on information compiled from our fieldwork, the scientific literature, technical reports, museum collections and interviews, we found evidence for up to 13 xenarthran species occurring in the STNF (Table 1). The geographic distribution of ten of them suggests their occurrence in the study area. The other three were mentioned only in the two technical reports; they have yet to be confirmed, and may be erroneous. Fieldwork We found six xenarthran species in our field surveys, three of them in reforested areas (Table 1). We recorded three of the four known species of anteaters in the study area. Three giant anteaters (Myrmecophaga tridactyla) were seen in the reforested areas, twice in plots reforested in the 1980s and once in a plot from the 1990s. The southern tamandua (Tamandua tetradactyla) was seen on six occasions, four of which were in the remaining forest of the Almeidas plateau. We found a fifth individual dead in the 1990s reforested plot, showing unmistakable signs of predation broken bones, bite marks on the head, and large parts of the body missing. The sixth was found dead on the road between Porto de Trombetas and the Almeidas plateau, probably killed by a vehicle. We also found a pygmy anteater (Cyclopes didactylus) killed on the same road. There are two species of sloth in the STNF: the pale-throated three-toed sloth (Bradypus tridactylus: Bradypodidae) and the two-toed sloth (Choloepus didactylus: Megalonychidae). A three-toed sloth was found dead on the road, and an IBAMA technician observed another crossing the road at Porto de Trombetas. Choloepus didactylus was the most frequently sighted of the xenarthrans during our field study, with a total of ten records for this species six of which were dead specimens found on the road. We recorded just one species of armadillo, the common long-nosed armadillo (Dasypus novemcinctus). We saw one in the Almeidas forest, and a second in the 1980s reforested zone at Saracá; a third was found dead on the road to Porto de Trombetas. Museum collections There are specimens of two xenarthran species from the STNF in the mammal collection of the Museu Paraense Emílio Goeldi: two of Bradypus variegatus (Faro and headwaters of the Rio Paru do Oeste), and one of the greater long-nosed armadillo, Dasypus kappleri, collected from the Rio Saracazinho, Porto Trombetas (Table 1). 4 Edentata no. 7 May 2006

Interviews and published literature The presence of the giant armadillo (Priodontes maximus) was inferred by its burrows (recorded by an IBAMA technician, Antônio de Almeida Correia) and it was also listed during inventories for an environmental impact statement (Brandt Meio Ambiente, 2001) and for the preparation of a management plan for the national forest (STCP, 2001). The Brazilian lesser long-nosed armadillo (Dasypus septemcinctus) may also be present, as one of the technicians we interviewed described two different species of armadillos, one with nine bands in the carapace and the other with seven. The technician was unable to identify the exact species from the illustrations we provided, however, and this record is provisional. The southern naked-tail armadillo (Cabassous unicinctus), the Brazilian three-banded armadillo (Tolypeutes tricinctus) and the yellow armadillo (Euphractus sexcinctus) were only recorded in some publications and technical reports (Table 1). Discussion Although our study registered a potential total of 13 xenarthran species in the Saracá-Taquera National Forest, not all have been verified. The Brazilian threebanded armadillo (Tolypeutes tricinctus), although listed in a technical report (STCP, 2001) is unlikely to occur in the study area. It has never been recorded in Amazonia, and occurs mainly in the Cerrado biome (Wetzel, 1982, 1985a; Fonseca et al., 1996; Eisenberg and Redford, 1999). The presence of the yellow armadillo (Euphractus sexcinctus) also remains to be confirmed. According to Wetzel (1985a), this species occurs in northeastern, middle-western, southeastern, and southern Brazil, but Silva Júnior and Nunes (2001) and Silva Júnior et al. (2001) have found it in the eastern Amazon, and proposed that its disjunct range is an artifact of sampling. Our records for this species are based only on interviews and technical reports. TABLE 1. Edentate fauna reported from the Saracá-Taquera National Forest, Pará, Brazil, from scientific collections, published reports and fieldwork. The number of individuals observed is given in parentheses. Order Edentata Museum Literature Fieldwork MPEG Technical reports Scientific papers Mature forest Reforested area Myrmecophagidae Myrmecophaga tridactyla 1, 2 1, 3, 4, 5 Obs. (3) Tamandua tetradactyla 1, 2 1, 3, 4, 5 Obs. (4) Obs. (1) Obs.(1) Cyclopes didactylus 1, 2 1, 3, 4, 5 Obs. (1) Bradypodidae Bradypus tridactylus 1, 3, 4, 5 Obs.(2) Bradypus variegatus* 304; 1743 1, 2 1, 3, 5 Megalonychidae Choloepus didactylus 1, 2 1, 3, 4, 5 Obs. (4) Obs.(6) Dasypodidae Priodontes maximus 1, 2 1, 2, 3, 4, 5 Int. Cabassous unicinctus 1, 2 1, 2, 3, 4, 5 Tolypeutes tricinctus** 1 Dasypus kappleri*** 12592 1, 2, 3, 4, 5 Dasypus novemcinctus 1, 2, 3, 4, 5 Obs (1) Obs. (1) Obs. (1) Dasypus septemcinctus**** Int. Euphractus sexcinctus 1, 2 Literature: 1 Wetzel, 1982; 2 Wetzel, 1985a; 3 Wetzel, 1985b; 4 Emmons and Feer, 1997; 5 Eisenberg and Redford, 1999. Technical reports: 1. STCP, 2001; 2. Brandt Meio Ambiente, 2001. * MPEG 304: Faro and MPEG 1743: Cabeceiras do Rio Paru de Oeste. ** Improbable occurrence due to a geographic range restricted to other biomes. *** MPEG 12592: Rio Saracazinho, Porto Trombetas. **** Species recorded by interview and recorded in the Porto Trombetas Biological Reserve. Obs. = Direct observation of the species. Int. = Interview. Road 5

Dasypus septemcinctus has yet to be confirmed for the STNF. It has a broad range, from the mouth of the Amazon to the Gran Chaco in Argentina (Wetzel, 1985b), but none have been recorded from the central Amazon. As mentioned above, the presence of this species was suggested by one of the technicians we interviewed, and D. septemcinctus was listed in the management plan for the Rio Trombetas Biological Reserve, on the east side of the Rio Trombetas (Antônio de Almeida Correia, pers. comm.). Thus, we consider its occurrence possible for the STNF, but we have no concrete evidence of it having been seen or collected there. Three of the six species recorded in our fieldwork two anteaters (Myrmecophaga tridactyla and Tamandua tetradactyla) and an armadillo (Dasypus novemcinctus) were seen in reforested areas. These areas appear to be important for the xenarthran fauna at Porto de Trombetas; the giant anteater (M. tridactyla), for instance, was only recorded in these areas. This may have been due to easier visibility in those areas; but field studies will be necessary to determine how these reforested areas support the local xenarthran fauna, and how xenarthrans colonize reforested patches. The principal threats facing the xenarthran fauna of this region are hunting and roads. Road mortality has been considered one of the worst dangers to terrestrial fauna (Forman and Alexander, 1998), and all six of the species that we directly observed were found dead on the road. Xenarthrans are more vulnerable to highway traffic than most other mammals, as many of them have poor vision and are not equipped for a fast escape. Edentates are a favored source of meat throughout the Neotropics (Redford, 1992; Leeuwenberg, 1997; Cullen et al., 2000; Peres, 2000; Valsecchi, 2005), and many people in the STNF hunt wild game for food. Interviews with our field assistants indicated a strong preference for the armadillos, and our assistants showed us the carapaces of some recent kills. Despite the road casualties and local hunting, the Saracá-Taquera National Forest has a remarkable richness of xenarthran species. This gives it a special importance as a protected area, and makes it an excellent location to study the dynamics of mammal recolonization in regenerating tropical forest. Acknowledgements: We thank the Brazilian Institute of Environment and Renewable Natural Resources (IBAMA), Porto de Trombetas, Pará, for permission to work in the Saracá-Taquera National Forest; Antônio de Almeida Correia (IBAMA) for useful information; our colleagues from the Horto Florestal; Rio do Norte Mining Company (MRN) for logistical help, especially Alexandre Castilho; and Leonardo Viana and Lyn Buchheit for the English corrections. Rio do Norte Mining Company (MRN) and Planta Ltda. funded this study. The first author thanks CAPES/ Fulbright for the fellowship in support of his doctoral studies at the University of Maryland. Leonardo de Carvalho Oliveira, Graduate Program in Biology, University of Maryland, College Park, MD 20742, USA, e-mail: <leoecol@umd.edu>, Sylvia Miscow Mendel, Pós-Graduação em Ecologia Conservação e Manejo da Vida Silvestre, ICB, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, Pampulha, Belo Horizonte 30270-901, Minas Gerais, Brazil, e-mail: <smmendel@terra. com.br>, Diogo Loretto, Programa de Pós-Graduação em Ecologia, Universidade Federal do Rio de Janeiro, CP 68020, Av. Brigadeiro Trompovsky s/n, Ilha do Fundão, Rio de Janeiro 21941-590, Rio de Janeiro, Brazil, e-mail: <diogoloretto@yahoo.com. br>, José de Sousa e Silva Júnior, Setor de Mastozoologia, Coordenação de Zoologia, Museu Paraense Emílio Goeldi, CP 399, Belém 66040-170, Pará, Brazil, e-mail: <cazuza@museu-goeldi.br>, and Geraldo Wilson Fernandes, Planta Ltda. and Ecologia Evolutiva de Herbívoros Tropicais / DBG, ICB, Universidade Federal de Minas Gerais, CP 486, Belo Horizonte 30270-901, Minas Gerais, Brazil, e-mail: <gwilson@icb.ufmg.br>. References Brandt Meio Ambiente. 2001. Estudos de Impacto Ambiental Platô Almeidas. Unpublished report. Mineração Rio do Norte, Porto de Trombetas, Oriximiná, Pará. Cullen Jr., L., Bodmer, R. E. and Valladares-Pádua, C. 2000. Effects of hunting in habitat fragments of the Atlantic forests, Brazil. Biological Conservation 95: 49 56. Eisenberg, J. F. and Redford, K. H. 1999. Mammals of the Neotropics, Volume 3: The Central Neotropics: Ecuador, Peru, Bolivia, Brazil. The University of Chicago Press, Chicago. Emmons, L. H. and Feer, F. 1997. Neotropical Rainforest Mammals: A Field Guide. Second edition. The University of Chicago Press, Chicago. Fonseca, G. A. B. da, Hermann, G., Leite, Y. L. R., Mittermeier, R. A., Rylands, A. B. and Patton, J. L. 1996. Lista anotada dos mamíferos do Brasil. Occasional Papers in Conservation Biology 4: 1 38. Conservation International and Fundação Biodiversitas, Washington, DC. 6 Edentata no. 7 May 2006

Fonseca, G. A. B. da. 2001. The conservation of xenarthra will be vital for the preservation of mammalian phylogenetic diversity. Edentata (4): 1. Fonseca, G. A. B. da and Aguiar, J. M. 2004. The 2004 Edentate Species Assessment Workshop. Edentata (6): 1 26. Fonseca, G. A. B. da and Chiarello, A. G. 2003. Official list of Brazilian fauna threatened with extinction 2002. Edentata (5): 56 59. Forman, R. T. T. and Alexander, L. E. 1998. Roads and their major ecological effects. Ann. Rev. Ecol. Syst. 29: 207 231. Leeuwenberg, F. 1997. Edentata as a food resource: Subsistence hunting by Xavante Indians, Brazil. Edentata (3): 4 5. Murphy, W. J., Eizirik, E., Johnson, W. E., Zhang, Y. P., Ryder, O. A. and O Brien, S. J. 2001. Molecular phylogenetics and the origins of placental mammals. Nature 409: 614 618. Peres, C. A. 2000. Effects of subsistence hunting on vertebrate community structure in Amazonian forest. Conservation Biology 14(1): 240 253. Redford, K. H. 1992. The empty forest. BioScience 42: 412 422. Silva Júnior, J. S. and Nunes, A. P. 2001. Disjunct geographical distribution of the yellow armadillo, Euphractus sexcinctus (Xenarthra: Dasypodidae). Edentata (4): 16 18. Silva Júnior, J. S., Fernandes, M. E. B. and Cerqueira, R. 2001. New records of the yellow armadillo, Euphractus sexcinctus (Xenarthra: Dasypodidae) in the state of Maranhão, Brazil. Edentata (4): 18 23. STCP. 2001. Plano de Manejo da Floresta Nacional de Saracá-Taquera, Estado do Pará, Brasil. Unpublished report. STCP Engenharia, Consultoria e Gerenciamento, Curitiba, Paraná. Valsecchi, J. A. 2005. Diversidade de mamíferos não voadores e uso da fauna nas Reservas de Desenvolvimento Sustentável Mamirauá e Amanã, Amazonas, Brasil. Master s thesis, Programa de Pós-Graduação em Zoologia, Museu Paraense Emílio Goeldi and Universidade Federal do Pará, Belém. Wetzel, R. M. 1982. Systematics, distribution, ecology, and conservation of South American Edentates. In: Mammalian Biology in South America, M. A. Mares and H. H. Genoways (eds.), pp. 345 375. Special Publication Series of the Pymatuning Laboratory of Ecology, University of Pittsburgh, Pittsburgh. Wetzel, R. M. 1985a. The identification and distribution of recent Xenarthra (= Edentata). In: The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas, G. G. Montgomery (ed.), pp.5 21. Smithsonian Institution Press, Washington, DC. Wetzel, R. M. 1985b. Taxonomy and distribution of armadillos, Dasypodidae. In: The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas, G. G. Montgomery (ed.), pp.23 46. Smithsonian Institution Press, Washington, DC. A Southern Extension of the Geographic Distribution of the Two-Toed Sloth, Choloepus didactylus (Xenarthra, Megalonychidae) Cristiano Trapé Trinca Francesca Belem Lopes Palmeira José de Sousa e Silva Júnior The two species of two-toed sloths, Choloepus didactylus and C. hoffmanni, are the only extant representatives of the Megalonychidae (Adam, 1999), occurring in partial sympatry in the Andean regions and western Amazonia (Le Pont and Desjeux, 1992; Emmons and Feer, 1997; Adam, 1999; Eisenberg and Redford, 1999). Although their distributions are reasonably well-understood on a broad scale, the precise boundaries of their ranges are still unresolved. According to Wetzel and Ávila-Pires (1980), Wetzel (1985), Adam (1999) and Eisenberg and Redford (1999), C. didactylus occurs across all of northern Amazonia, from the eastern Andes to northeastern Surinam, reaching the northern coast of Brazil in the states of Amapá, Pará and Maranhão. The maps presented by Wetzel (1985), Emmons and Feer (1997) and Eisenberg and Redford (1999) all suggest that in Western Amazonia, this distribution extends southward to 10 S latitude. In central and eastern Amazonia, however, their maps show Choloepus didactylus as being restricted to a narrow belt along the southern edge of the Amazon River although there is no ecological reason why the species might not occur further to the south. Wetzel and Ávila-Pires (1980) reported the only records for this region available at the time, referring to specimens from Santarém, Taperinha and Rio Barcarena in Pará, as well as Humberto de Campos in Maranhão. Specimens in the mammal collection of the Museu Paraense Emílio Goeldi (MPEG) confirm this distribution, including those from the following localities in eastern Pará: Marituba (MPEG 22070), Paragominas (MPEG 30677), Fazenda Cauaxi, municipality of Paragominas (MPEG 26315, 26316, 26317), and Rodovia Belém-Brasília, Km- 75 (MPEG 2385, 2391, 2394). With the exception of the last three individuals, all these specimens were collected after 1980 and were thus not available to Wetzel and Ávila-Pires. 7